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Maternal protein malnutrition: effects on prostate development and adult disease

Part of: French DOHaD

Published online by Cambridge University Press:  27 March 2018

J. C. Rinaldi ,
S. A. A. Santos ,
K. T. Colombelli ,
L. Birch ,
G. S. Prins ,
L. A. Justulin Jr  and
S. L. Felisbino
J. C. Rinaldi*
Affiliation:
Department of Morphological Sciences, Biological Sciences Center, State University of Maringa (UEM), Maringa, PR, Brazil Department of Morphology, Institute of Biosciences, Sao Paulo State University (UNESP), Botucatu, SP, Brazil Department of Urology, University of Illinois at Chicago (UIC), Chicago, IL, USA
S. A. A. Santos
Affiliation:
Department of Morphology, Institute of Biosciences, Sao Paulo State University (UNESP), Botucatu, SP, Brazil
K. T. Colombelli
Affiliation:
Department of Morphology, Institute of Biosciences, Sao Paulo State University (UNESP), Botucatu, SP, Brazil
L. Birch
Affiliation:
Department of Urology, University of Illinois at Chicago (UIC), Chicago, IL, USA
G. S. Prins
Affiliation:
Department of Urology, University of Illinois at Chicago (UIC), Chicago, IL, USA
L. A. Justulin Jr
Affiliation:
Department of Morphology, Institute of Biosciences, Sao Paulo State University (UNESP), Botucatu, SP, Brazil
S. L. Felisbino
Affiliation:
Department of Morphology, Institute of Biosciences, Sao Paulo State University (UNESP), Botucatu, SP, Brazil
*
Address for correspondence: Dr J. C Rinaldi, Departamento de Ciências Morfológicas, Universidade Estadual de Maringá (UEM), Av. Colombo 5900, bloco H-79, sala 105B, Maringá, PR, CEP 87020-900, Brazil. E-mail: jak.rinaldi@gmail.com
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Abstract

Well-controlled intrauterine development is an essential condition for many aspects of normal adult physiology and health. This process is disrupted by poor maternal nutrition status during pregnancy. Indeed, physiological adaptations occur in the fetus to ensure nutrient supply to the most vital organs at the expense of the others, leading to irreversible consequences in tissue formation and differentiation. Evidence indicates that maternal undernutrition in early life promotes changes in key hormones, such as glucocorticoids, growth hormones, insulin-like growth factors, estrogens and androgens, during fetal development. These alterations can directly or indirectly affect hormone release, hormone receptor expression/distribution, cellular function or tissue organization, and impair tissue growth, differentiation and maturation to exert profound long-term effects on the offspring. Within the male reproductive system, maternal protein malnutrition alters development, structure, and function of the gonads, testes and prostate gland. Consequently, these changes impair the reproductive capacity of the male offspring. Further, permanent alterations in the prostate gland occur at the molecular and cellular level and thereby affect the onset of late life diseases such as prostatitis, hyperplasia and even prostate cancer. This review assembles current thoughts on the concepts and mechanisms behind the developmental origins of health and disease as they relate to protein malnutrition, and highlights the effects of maternal protein malnutrition on rat prostate development and homeostasis. Such insights on developmental trajectories of adult-onset prostate disease may help provide a foundation for future studies in this field.

Keywords

fetal programminglow-protein dietandrogen receptorprostatitis
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 9 , Issue 4: Themed Issue: French DOHaD , August 2018 , pp. 361 - 372
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2018 

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References

1. Black, RE, Allen, LH, Bhutta, ZA, et al. Maternal and child undernutrition: global and regional exposures and health consequences. Lancet. 2008; 371, 243–260.Google Scholar
2. World Health Organization. Malnutrition. Retrieved 14 October 2017 from http://www.who.int/mediacentre/factsheets/malnutrition/en/ Google Scholar
3. Manolio, TA, Collins, FS, Cox, NJ, et al. Finding the missing heritability of complex diseases. Nature. 2009; 461, 747–753.Google Scholar
4. Tain, Y-L, Huang, L-T, Hsu, C-N. Developmental programming of adult disease: reprogramming by melatonin? Int J Mol Sci. 2017; 18, 426–438.Google Scholar
5. Barker, DJ. Maternal nutrition, fetal nutrition, and disease in later life. Nutrition. 1997; 13, 807–813.Google Scholar
6. Bennis-Taleb, N, Remacle, C, Hoet, JJ, Reusens, B. A low-protein isocaloric diet during gestation affects brain development and alters permanently cerebral cortex blood vessels in rat offspring. J Nutr. 1999; 129, 1613–1619.Google Scholar
7. Gluckman, PD, Hanson, MA. The developmental origins of the metabolic syndrome. Trends Endocrinol Metab. 2004; 15, 183–187.Google Scholar
8. Barker, DJP. The origins of the developmental origins theory. J Intern Med. 2007; 261, 412–417.Google Scholar
9. Habib, S, Zhang, Q, Baum, M. Prenatal programming of hypertension in the rat: effect of postnatal rearing. Nephron Extra. 2011; 1, 157–165.Google Scholar
10. Nijland, MJ, Ford, SP, Nathanielsz, PW. Prenatal origins of adult disease. Curr Opin Obstet Gynecol. 2008; 20, 132–138.Google Scholar
11. Boeri, L, Ventimiglia, E, Capogrosso, P, et al. Low birth weight is associated with a decreased overall adult health status and reproductive capability – results of a cross-sectional study in primary infertile patients. PLoS One. 2016; 11, e0166728.Google Scholar
12. Langley-Evans, SC, Sculley, DV. The association between birthweight and longevity in the rat is complex and modulated by maternal protein intake during fetal life. FEBS Lett. 2006; 580, 4150–4153.Google Scholar
13. Warner, MJ, Ozanne, SE. Mechanisms involved in the developmental programming of adulthood disease. Biochem J. 2010; 427, 333–347.Google Scholar
14. Kalhan, SC, Wilson-Costello, D. Prematurity and programming: contribution of neonatal intensive care unit interventions. J Dev Orig Health Dis. 2013; 4, 121–133.Google Scholar
15. Roseboom, TJ, Van Der Meulen, JH, Ravelli, AC, et al. Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview. Twin Res. 2001; 4, 293–298.Google Scholar
16. McMillen, IC, Robinson, JS. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiolo Rev. 2005; 85, 571–633.Google Scholar
17. Vangen, S, Nordhagen, R, Lie, KK. Revisiting the Forsdahl-Barker hypothesis. Tidsskr Nor Laegeforen. 2005; 125, 451–453.Google Scholar
18. Langley-Evans, SC, McMullen, S. Developmental origins of adult disease. Med Princ Pract. 2010; 19, 87–98.Google Scholar
19. Langley-Evans, SC. Nutritional programming of disease: unravelling the mechanism. J Anat. 2009; 215, 36–51.Google Scholar
20. Barker, DJ, Gluckman, PD, Godfrey, KM, et al. Fetal nutrition and cardiovascular disease in adult life. Lancet. 1993; 341, 938–941.Google Scholar
21. Fowden, AL, Forhead, AJ. Hormones as epigenetic signals in developmental programming. Exp Physiol. 2009; 94, 607–625.Google Scholar
22. Vuguin, PM. Animal models for small for gestational age and fetal programing of adult disease. Horm Res. 2007; 68, 113–123.Google Scholar
23. Vaiserman, A. Epidemiologic evidence for association between adverse environmental exposures in early life and epigenetic variation: a potential link to disease susceptibility? Clin Epigenetics. 2015; 7, 96.Google Scholar
24. Jiang, Y, Sun, T, Xiong, J, et al. Hyperhomocysteinemia-mediated DNA hypomethylation and its potential epigenetic role in rats. Acta Biochim Biophys Sin. 2007; 39, 657–667.Google Scholar
25. Wu, G, Imhoff-Kunsch, B, Girard, AW. Biological mechanisms for nutritional regulation of maternal health and fetal development. Paediatr Perinat Epidemiol. 2012; 26, 4–26.Google Scholar
26. Langley-Evans, SC. Nutrition in early life and the programming of adult disease: a review. J Hum Nutr Diet. 2015; 28, 1–14.Google Scholar
27. Jahan-Mihan, A, Rodriguez, J, Christie, C, Sadeghi, M, Zerbe, T. The role of maternal dietary proteins in development of metabolic syndrome in offspring. Nutrients. 2015; 7, 9185–9217.Google Scholar
28. Dai, Z, Wu, Z, Hang, S, Zhu, W, Wu, G. Amino acid metabolism in intestinal bacteria and its potential implications for mammalian reproduction. Mol Hum Reprod. 2015; 21, 389–409.Google Scholar
29. Chadio, S, Kotsampasi, B. Maternal undernutrition and developmental programming: implications for offspring reproductive potential. In Handbook of famine, starvation, and nutrient deprivation (eds. Preedy V, Patel V), 2017; pp. 1–17. Springer International Publishing: New York, NY.Google Scholar
30. Benevenga, NJ, Calvert, C, Eckhert, CD, et al. Nutrient Requirements of the Laboratory Rats, 4th edn, 1995; pp. 11–79. National Academy Press: Washington, DC.Google Scholar
31. Cahill, GF. Fuel metabolism in starvation. Ann Rev Nutr. 2006; 26, 1–22.Google Scholar
32. Zambrano, E, Rodríguez-González, GL, Guzmán, C, et al. A maternal low protein diet during pregnancy and lactation in the rat impairs male reproductive development. J Physiol. 2005; 563, 275–284.Google Scholar
33. Zambrano, E, Bautista, CJ, Deás, M, et al. A low maternal protein diet during pregnancy and lactation has sex- and window of exposure-specific effects on offspring growth and food intake, glucose metabolism and serum leptin in the rat. J Physiol. 2006; 571, 221–230.Google Scholar
34. Aihie Sayer, A, Dunn, R, Langley-Evans, S, Cooper, C. Prenatal exposure to a maternal low protein diet shortens life span in rats. Gerontology. 2001; 47, 9–14.Google Scholar
35. Brameld, JM, Buttery, PJ, Dawson, JM, Harper, JM. Nutritional and hormonal control of skeletal-muscle cell growth and differentiation. Proc Nutr Soc. 1998; 57, 207–217.Google Scholar
36. Vicente, LL, de Moura, EG, Lisboa, PC, et al. Malnutrition during lactation in rats is associated with higher expression of leptin receptor in the pituitary of adult offspring. Nutrition. 2004; 20, 924–928.Google Scholar
37. Lins, MC, de Moura, EG, Lisboa, PC, Bonomo, IT, Passos, MCF. Effects of maternal leptin treatment during lactation on the body weight and leptin resistance of adult offspring. Regul Pept. 2005; 127, 197–202.Google Scholar
38. Colombelli, KT, Santos, SAA, Camargo, ACL, et al. Impairment of microvascular angiogenesis is associated with delay in prostatic development in rat offspring of maternal protein malnutrition. Gen Comp Endocrinol. 2017; 246, 258–269.Google Scholar
39. Hou, Y, Yin, Y, Wu, G. Dietary essentiality of ‘nutritionally non-essential amino acids’ for animals and humans. Exp Biol Med. 2015; 240, 997–1007.Google Scholar
40. Jahan-Mihan, A, Szeto, IMY, Luhovyy, BL, Huot, PSP, Anderson, GH. Soya protein- and casein-based nutritionally complete diets fed during gestation and lactation differ in effects on characteristics of the metabolic syndrome in male offspring of Wistar rats. Br J Nutr. 2012; 107, 284–294.Google Scholar
41. Kalhan, SC. One carbon metabolism in pregnancy: impact on maternal, fetal and neonatal health. Mol Cell Endocrinol. 2016; 435, 48–60.Google Scholar
42. Langley-Evans, SC. Fetal origins of adult disease. Br J Nutr. 1999; 81, 5–6.Google Scholar
43. Ozanne, SE, Wang, CL, Coleman, N, Smith, GD. Altered muscle insulin sensitivity in the male offspring of protein-malnourished rats. Am J Physiol. 1996; 271, 1128–1134.Google Scholar
44. Kalhan, SC, Uppal, SO, Moorman, JL, et al. Metabolic and genomic response to dietary isocaloric protein restriction in the rat. J Biol Chem. 2011; 286, 5266–5277.Google Scholar
45. Jackson, AA, Dunn, RL, Marchand, MC, Langley-Evans, SC. Increased systolic blood pressure in rats induced by a maternal low-protein diet is reversed by dietary supplementation with glycine. Clin Sci. 2002; 103, 633–639.Google Scholar
46. Steegers-Theunissen, RPM, Steegers, EAP. Nutrient-gene interactions in early pregnancy: a vascular hypothesis. Eur J Obstet Gynecol Reprod Biol. 2003; 106, 115–117.Google Scholar
47. Cherif, H, Reusens, B, Ahn, MT, Hoet, JJ, Remacle, C. Effects of taurine on the insulin secretion of rat fetal islets from dams fed a low-protein diet. J Endocrinol. 1998; 159, 341–348.Google Scholar
48. Sanders, LM, Zeisel, SH. Choline. Nutr Today. 2007; 42, 181–186.Google Scholar
49. Pupovac, J, Anderson, GH. Dietary peptides induce satiety via cholecystokinin-A and peripheral opioid receptors in rats. J Nutr. 2002; 132, 2775–2780.Google Scholar
50. Teschemacher, H. Opioid receptor ligands derived from food proteins. Curr Pharm Des. 2003; 9, 1331–1344.Google Scholar
51. Clare, DA, Swaisgood, HE. Bioactive milk peptides: a prospectus. J Dairy Sci. 2000; 83, 1187–1195.Google Scholar
52. Nielsen, SD, Beverly, RL, Qu, Y, Dallas, DC. Milk bioactive peptide database: a comprehensive database of milk protein-derived bioactive peptides and novel visualization. Food Chem. 2017; 232, 673–682.Google Scholar
53. Bos, C, Metges, CC, Gaudichon, C, et al. Postprandial kinetics of dietary amino acids are the main determinant of their metabolism after soy or milk protein ingestion in humans. J Nutr. 2003; 133, 1308–1315.Google Scholar
54. Tang, JE, Moore, DR, Kujbida, GW, Tarnopolsky, MA, Phillips, SM. Ingestion of whey hydrolysate, casein, or soy protein isolate: effects on mixed muscle protein synthesis at rest and following resistance exercise in young men. J Appl Physiol. 2009; 107, 987–992.Google Scholar
55. Cleal, JK, Lewis, RM. The mechanisms and regulation of placental amino acid transport to the human foetus. J Neuroendocrinol. 2008; 20, 419–426.Google Scholar
56. Carter, AM, Mess, A. Evolution of the placenta in eutherian mammals. Placenta. 2007; 28, 259–262.Google Scholar
57. Poston, L. Endothelial dysfunction in pre-eclampsia. Pharmacol Rep. 2006; 58, 69–74.Google Scholar
58. Fowden, AL, Forhead, AJ. Endocrine mechanisms of intrauterine programming. Reproduction. 2004; 127, 515–526.Google Scholar
59. Koopman, P. Organogenesis in Development. 2010. Academic Press: Cambridge, MA.Google Scholar
60. Bateson, P, Barker, D, Clutton-Brock, T, et al. Developmental plasticity and human health. Nature. 2004; 430, 419–421.Google Scholar
61. Cohen, E, Baerts, W, Bel, F. Brain-sparing in intrauterine growth restriction: considerations for the neonatologist. Neonatology. 2015; 108, 269–276.Google Scholar
62. Jee, Y-H, Baron, J, Phillip, M, Bhutta, ZA. Malnutrition and catch-up growth during childhood and puberty. World Rev Nutr Diet. 2014; 109, 89–100.Google Scholar
63. Ong, KK, Ahmed, ML, Emmett, PM, Preece, MA, Dunger, DB. Association between postnatal catch-up growth and obesity in childhood: prospective cohort study. BMJ. 2000; 320, 967–971.Google Scholar
64. Norris, SA, Osmond, C, Gigante, D, et al. Size at birth, weight gain in infancy and childhood, and adult diabetes risk in five low- or middle-income country birth cohorts. Diabetes Care. 2012; 35, 72–79.Google Scholar
65. Luo, L, Wang, Y, Feng, Q, et al. Recombinant protein glutathione S-transferases P1 attenuates inflammation in mice. Mol Immunol. 2009; 46, 848–857.Google Scholar
66. Tarry-Adkins, JL, Ozanne, SE. Mechanisms of early life programming: current knowledge and future directions. Am J Clin Nutr. 2011; 94, 1765S–1771S.Google Scholar
67. Luo, ZC, Fraser, WD, Julien, P, et al. Tracing the origins of ‘fetal origins’ of adult diseases: programming by oxidative stress? Med Hypotheses. 2006; 66, 38–44.Google Scholar
68. Lenzen, S. Oxidative stress: the vulnerable beta-cell. Biochem Soc Trans. 2008; 36, 343–347.Google Scholar
69. Dunford, LJ, Sinclair, KD, Kwong, WY, et al. Maternal protein-energy malnutrition during early pregnancy in sheep impacts the fetal ornithine cycle to reduce fetal kidney microvascular development. FASEB J. 2014; 28, 4880–4892.Google Scholar
70. Habib, S, Zhang, Q, Baum, M. Prenatal programming of hypertension in the rat: effect of postnatal rearing. Nephron Extra. 2011; 1, 157–165.Google Scholar
71. Dahri, S, Snoeck, A, Reusens-Billen, B, Remacle, C, Hoet, JJ. Islet function in offspring of mothers on low-protein diet during gestation. Diabetes. 1991; 40, 115–120.Google Scholar
72. Bennis-Taleb, N, Remacle, C, Hoet, JJ, Reusens, B. A low-protein isocaloric diet during gestation affects brain development and alters permanently cerebral cortex blood vessels in rat offspring. J Nutr. 1999; 129, 1613–1619.Google Scholar
73. Plagemann, A, Harder, T, Rake, A, et al. Hypothalamic nuclei are malformed in weanling offspring of low protein malnourished rat dams. J Nutr. 2000; 130, 2582–2589.Google Scholar
74. Farid, SA, Mahmoud, OM, Salem, NA, Abdel-Alrahman, G, Hafez, GA. Long term effects of maternal protein restriction on postnatal lung alveoli development of rat offspring. Folia Morphol. 2015; 74, 479–485.Google Scholar
75. Burns, SP, Desai, M, Cohen, RD, et al. Gluconeogenesis, glucose handling, and structural changes in livers of the adult offspring of rats partially deprived of protein during pregnancy and lactation. J Clin Invest. 1997; 100, 1768–1774.Google Scholar
76. Simmons, RA, Gounis, AS, Bangalore, SA, Ogata, ES. Intrauterine growth retardation: fetal glucose transport is diminished in lung but spared in brain. Pediatr Res. 1992; 31, 59–63.Google Scholar
77. Simmons, RA, Flozak, AS, Ogata, ES. The effect of insulin and insulin-like growth factor-I on glucose transport in normal and small for gestational age fetal rats. Endocrinology. 1993; 133, 1361–1368.Google Scholar
78. Barker, DJP, Osmond, C, Forsén, TJ, Kajantie, E, Eriksson, JG. Trajectories of growth among children who have coronary events as adults. N Engl J Med. 2005; 353, 1802–1809.Google Scholar
79. Gluckman, PD, Hanson, MA. The developmental origins of the metabolic syndrome. Trends Endocrinol Metab. 2004; 15, 183–187.Google Scholar
80. Bertram, CE, Hanson, MA. Animal models and programming of the metabolic syndrome. Br Med Bull. 2001; 60, 103–121.Google Scholar
81. Qasem, RJ, Yablonski, E, Li, J, et al. Elucidation of thrifty features in adult rats exposed to protein restriction during gestation and lactation. Physiol Behav. 2012; 105, 1182–1193.Google Scholar
82. Ozanne, SE, Hales, CN. Early programming of glucose-insulin metabolism. Trends Endocrinol Metab. 2002; 13, 368–373.Google Scholar
83. Rowe, PJ, Comhaire, FH, Hargreave, TB, Mellows, HJ. WHO Manual for the Standard Investigation and Diagnosis of the Infertile Couple . 1993. Cambridge University Press: Cambridge.Google Scholar
84. Chow, V, Cheung, AP. Male infertility. J Reprod Med. 2003; 3, 149–156.Google Scholar
85. Francois, I, de Zegher, F, Spiessens, C, d’Hooghe, T, Vanderschueren, D. Low birth weight and subsequent male subfertility. Pediatr Res. 1997; 42, 899–901.Google Scholar
86. Cicognani, A, Alessandroni, R, Pasini, A, et al. Low birth weight for gestational age and subsequent male gonadal function. J Pediatr. 2002; 3, 376–379.Google Scholar
87. Vanbillemont, G, Lapauw, B, Bogaert, V, et al. Birth weight in relation to sex steroid status and body composition in young healthy male siblings. J Clin Endocrinol Metab. 2010; 95, 1587–1594.Google Scholar
88. Léonhardt, M, Lesage, J, Croix, D, et al. 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. 2003; 68, 390–400.Google Scholar
89. Guzmán, C, Cabrera, R, Cárdenas, M, et al. Protein restriction during fetal and neonatal development in the rat alters reproductive function and accelerates reproductive ageing in female progeny. J Physiol. 2006; 572, 97–108.Google Scholar
90. Faria, TS, Brasil, FB, Sampaio, FJB, Ramos, CF. Maternal malnutrition during lactation alters the folliculogenesis and gonadotropins and estrogen isoforms ovarian receptors in the offspring at puberty. J Endocrinol. 2008; 198, 625–634.Google Scholar
91. Ramos, CF, Babinski, MA, Costa, WS, Sampaio, FJB. The prostate of weaned pups is altered by maternal malnutrition during lactation in rats. Asian J Androl. 2010; 12, 180–185.Google Scholar
92. Rhind, SM, Rae, MT, Brooks, AN. Effects of nutrition and environmental factors on the fetal programming of the reproductive axis. Reproduction. 2001; 122, 205–214.Google Scholar
93. Fowden, AL, Giussani, DA, Forhead, AJ. Intrauterine programming of physiological systems: causes and consequences. Physiology. 2006; 21, 29–37.Google Scholar
94. Rae, MT, Kyle, CE, Miller, DW, et al. The effects of undernutrition, in utero, on reproductive function in adult male and female sheep. Anim Reprod Sci. 2002; 72, 63–71.Google Scholar
95. McMillen, IC, MacLaughlin, SM, Muhlhausler, BS, et al. Developmental origins of adult health and disease: the role of periconceptional and foetal nutrition. Basic Clin Pharmacol Toxicol. 2008; 102, 82–89.Google Scholar
96. Gardner, DS, Ozanne, SE, Sinclair, KD. Effect of the early-life nutritional environment on fecundity and fertility of mammals. Philos Trans R Soc B Biol Sci. 2009; 364, 3419–3427.Google Scholar
97. Van Weissenbruch, MM, Engelbregt, MJT, Veening, MA, Delemarre-van de Waal, HA. Fetal nutrition and timing of puberty. Endocr Dev. 2005; 8, 15–33.Google Scholar
98. Noriega, NC, Howdeshell, KL, Furr, J, et al. Pubertal administration of DEHP delays puberty, suppresses testosterone production, and inhibits reproductive tract development in male Sprague-Dawley and Long-Evans rats. Toxicol Sci. 2009; 111, 163–178.Google Scholar
99. Rodríguez-González, GL, Vigueras-Villaseñor, RM, Millán, S, et al. Maternal protein restriction in pregnancy and/or lactation affects seminiferous tubule organization in male rat offspring. J Dev Orig Health Dis. 2012; 3, 321–326.Google Scholar
100. Asadi, N, Bahmani, M, Kheradmand, A, Rafieian-Kopaei, M. The impact of oxidative stress on testicular function and the role of antioxidants in improving it: a review. J Clin Diagn Res. 2017; 11, IE01–IE05.Google Scholar
101. Graham, S, Gandelman, R. The expression of ano-genital distance data in the mouse. Physiol Behav. 1986; 36, 103–104.Google Scholar
102. Swan, SH, Main, KM, Liu, F, et al. Decrease in anogenital distance among male infants with prenatal phthalate exposure. Environ Health Perspect. 2005; 113, 1056–1061.Google Scholar
103. Cunha, GR. Androgenic effects upon prostatic epithelium are mediated via trophic influences from stroma. Prog Clin Biol Res. 1984; 145, 81–102.Google Scholar
104. Verze, P, Cai, T, Lorenzetti, S. The role of the prostate in male fertility, health and disease. Nat Rev Urol. 2016; 13, 379–386.Google Scholar
105. Rinaldi, JC, Justulin, LA, Lacorte, LM, et al. Implications of intrauterine protein malnutrition on prostate growth, maturation and aging. Life Sci. 2013; 92, 763–774.Google Scholar
106. Fernandez-Twinn, DS, Ozanne, SE, Ekizoglou, S, et al. The maternal endocrine environment in the low-protein model of intra-uterine growth restriction. Br J Nutr. 2003; 90, 815–822.Google Scholar
107. Santos, AMS, Ferraz, MR, Teixeira, CV, Sampaio, FJB, Ramos, CF. Effects of undernutrition on serum and testicular testosterone levels and sexual function in adult rats. Horm Metab Res. 2004; 36, 27–33.Google Scholar
108. Fernandez-Twinn, DS, Ekizoglou, S, Gusterson, BA, Luan, J, Ozanne, SE. Compensatory mammary growth following protein restriction during pregnancy and lactation increases early-onset mammary tumor incidence in rats. Carcinogenesis. 2007; 28, 545–552.Google Scholar
109. Teixeira, CV, Silandre, D, de Souza Santos, AM, et al. Effects of maternal undernutrition during lactation on aromatase, estrogen, and androgen receptors expression in rat testis at weaning. J Endocrinol. 2007; 192, 301–311.Google Scholar
110. Ibrahim, MAA, Bayomy, NA, Elbakry, RH. Effects of maternal malnutrition during lactation on the prostate of rat offspring at puberty. Egypt J Histol. 2014; 37, 710–719.Google Scholar
111. Rodríguez-González, GL, Vigueras-Villaseñor, RM, Millán, S, et al. Maternal protein restriction in pregnancy and/or lactation affects seminiferous tubule organization in male rat offspring. J Dev Orig Health Dis. 2012; 3, 321–326.Google Scholar
112. Gombar, FM, Ramos, CF. Perinatal malnutrition programs gene expression of leptin receptors isoforms in testis and prostate of adult rats. Regul Pept. 2013; 184, 115–120.Google Scholar
113. Arrighi, S, Aralla, M, Genovese, P, Picabea, N, Bielli, A. Undernutrition during foetal to prepubertal life affects aquaporin 9 but not aquaporins 1 and 2 expression in the male genital tract of adult rats. Theriogenology. 2010; 74, 1661–1669.Google Scholar
114. Page, KC, Sottas, CM, Hardy, MP. Prenatal exposure to dexamethasone alters Leydig cell steroidogenic capacity in immature and adult rats. J Androl. 2001; 22, 973–980.Google Scholar
115. Untergasser, G, Madersbacher, S, Berger, P. Benign prostatic hyperplasia: age-related tissue-remodeling. Exp Geronto. 2005; 40, 121–128.Google Scholar
116. Risbridger, GP, Almahbobi, GA, Taylor, RA. Early prostate development and its association with late-life prostate disease. Cell Tissue Res. 2005; 322, 173–181.Google Scholar
117. Prins, GS, Huang, L, Birch, L, Pu, Y. The role of estrogens in normal and abnormal development of the prostate gland. Ann N Y Acad Sci. 2006; 1089, 1–13.Google Scholar
118. Cowin, PA, Foster, P, Pedersen, J, et al. Early-onset endocrine disruptor-induced prostatitis in the rat. Environ Health Perspect. 2008; 116, 923–929.Google Scholar
119. Prins, GS, Cooke, PS, Birch, L, et al. Androgen receptor expression and 5 alpha-reductase activity along the proximal-distal axis of the rat prostatic duct. Endocrinology. 1992; 130, 3066–3073.Google Scholar
120. Prins, GS, Putz, O. Molecular signaling pathways that regulate prostate gland development. Differentiation. 2008; 76, 641–659.Google Scholar
121. Timms, BG, Mohs, TJ, Didio, LJ. Ductal budding and branching patterns in the developing prostate. J Urol. 1994; 151, 1427–1432.Google Scholar
122. Prins, GS, Birch, L. The developmental pattern of androgen receptor expression in rat prostate lobes is altered after neonatal exposure to estrogen. Endocrinology. 1995; 136, 1303–1314.Google Scholar
123. Hayward, SW, Baskin, LS, Haughney, PC, et al. Epithelial development in the rat ventral prostate, anterior prostate and seminal vesicle. Acta Anat. 1996; 155, 81–93.Google Scholar
124. Marker, PC, Donjacour, AA, Dahiya, R, Cunha, GR. Hormonal, cellular, and molecular control of prostatic development. Dev Biol. 2003; 253, 165–174.Google Scholar
125. Lukacs, RU, Goldstein, AS, Lawson, DA, Cheng, D, Witte, ON. Isolation, cultivation and characterization of adult murine prostate stem cells. Nat Protoc. 2010; 5, 702–713.Google Scholar
126. Oliveira, DSM, Dzinic, S, Bonfil, AI, et al. The mouse prostate: a basic anatomical and histological guideline. Bosn J Basic Med Sci. 2016; 16, 8–13.Google Scholar
127. Sugimura, Y, Cunha, GR, Donjacour, AA. Morphogenesis of ductal networks in the mouse prostate. Biol Reprod. 1986; 34, 961–971.Google Scholar
128. Corbier, P, Edwards, DA, Roffi, J. The neonatal testosterone surge: a comparative study. Arch Int Physiol Biochim Biophys. 1992; 100, 127–131.Google Scholar
129. Welsh, M, Saunders, PTK, Fisken, M, et al. Identification in rats of a programming window for reproductive tract masculinization, disruption of which leads to hypospadias and cryptorchidism. J Clin Invest. 2008; 118, 1479–1490.Google Scholar
130. Imperato-McGinley, J, Zhu, Y-S. Androgens and male physiology the syndrome of 5alpha-reductase-2 deficiency. Mol Cell Endocrinol. 2002; 198, 51–59.Google Scholar
131. Toivanen, R, Shen, MM. Prostate organogenesis: tissue induction, hormonal regulation and cell type specification. Development. 2017; 144, 1382–1398.Google Scholar
132. Lu, W, Luo, Y, Kan, M, McKeehan, WL. Fibroblast growth factor-10. A second candidate stromal to epithelial cell andromedin in prostate. J Biol Chem. 1999; 274, 12827–12834.Google Scholar
133. Yan, G, Fukabori, Y, Nikolaropoulos, S, Wang, F, McKeehan, WL. Heparin-binding keratinocyte growth factor is a candidate stromal-to-epithelial-cell andromedin. Mol Endocrinol. 1992; 6, 2123–2128.Google Scholar
134. Timms, BG. Prostate development: a historical perspective. Differentiation. 2008; 76, 565–577.Google Scholar
135. Huang, L, Pu, Y, Birch, L, Prins, GS. Posterior Hox gene expression and differential androgen regulation in developing and adult rat prostate lobes. Endocrinology. 2007; 148, 1235–1245.Google Scholar
136. Huang, Z, Hurley, PJ, Simons, BW, et al. Sox9 is required for prostate development and prostate cancer initiation. Oncotarget. 2012; 3, 651–663.Google Scholar
137. DeGraff, DJ, Grabowska, MM, Case, TC, et al. FOXA1 deletion in luminal epithelium causes prostatic hyperplasia and alteration of differentiated phenotype. Lab Invest. 2014; 94, 726–739.Google Scholar
138. Dutta, A, Le Magnen, C, Mitrofanova, A, et al. Identification of an NKX3.1-G9a-UTY transcriptional regulatory network that controls prostate differentiation. Science. 2016; 352, 1576–1580.Google Scholar
139. Yu, M, Bushman, W. Differential stage-dependent regulation of prostatic epithelial morphogenesis by Hedgehog signaling. Dev Biol. 2013; 380, 87–98.Google Scholar
140. Pu, Y, Huang, L, Prins, G. Sonic hedgehog-patched Gli signaling in the developing rat prostate gland: lobe-specific suppression by neonatal estrogens reduces ductal growth and branching. Dev Biol. 2004; 273, 257–275.Google Scholar
141. McMahon, AP, Ingham, PW, Tabin, C. The developmental roles and clinical significance of Hedgehog signaling. Curr Top Dev Biol. 2003; 53, 1–114.Google Scholar
142 Freestone, SH, Marker, P, Grace, OC, et al. Sonic hedgehog regulates prostatic growth and epithelial differentiation. Dev Biol. 2003; 264, 352–362.Google Scholar
143. Prins, GS, Korach, KS. The role of estrogens and estrogen receptors in normal prostate growth and disease. Steroids. 2008; 73, 233–244.Google Scholar
144. Schenk, JM, Riboli, E, Chatterjee, N, et al. Serum retinol and prostate cancer risk: a nested case-control study in the prostate, lung, colorectal, and ovarian cancer screening trial. Cancer Epidemiol Biomarkers Prev. 2009; 18, 1227–1231.Google Scholar
145. Dagvadorj, A, Collins, S, Jomain, J-B, et al. Autocrine prolactin promotes prostate cancer cell growth via Janus kinase-2-signal transducer and activator of transcription-5a/b signaling pathway. Endocrinology. 2007; 148, 3089–3101.Google Scholar
146. Wang, Z, Prins, GS, Coschigano, KT, et al. Disruption of growth hormone signaling retards early stages of prostate carcinogenesis in the C3(1)/T antigen mouse. Endocrinology. 2005; 146, 5188–5196.Google Scholar
147. Powolny, AA, Wang, S, Carlton, PS, Hoot, DR, Clinton, SK. Interrelationships between dietary restriction, the IGF-I axis, and expression of vascular endothelial growth factor by prostate adenocarcinoma in rats. Mol Carcinog. 2008; 47, 458–465.Google Scholar
148. Fowden, AL. Endocrine regulation of fetal growth. Reprod Fertil Dev. 1995; 7, 351–363.Google Scholar
149. Zheng, J, Xiao, X, Zhang, Q, Wang, T, Yu, M, Xu, J. Maternal low-protein diet modulates glucose metabolism and hepatic microRNAs expression in the early life of offspring. Nutrients. 2017; 9, 205.Google Scholar
150. Walker, CL, Ho, S. Developmental reprogramming of cancer susceptibility. Nat Rev Cancer. 2012; 12, 479–486.Google Scholar
151. Wuidart, A, Ousset, M, Rulands, S, et al. Quantitative lineage tracing strategies to resolve multipotency in tissue-specific stem cells. Genes Dev. 2016; 30, 1261–1277.Google Scholar
152. Pignon, JC, Grisanzio, C, Geng, Y, et al. p63-expressing cells are the stem cells of developing prostate, bladder, and colorectal epithelia. Proc Natl Acad Sci. 2013; 110, 8105–8110.Google Scholar
153. Pinho, CF, Ribeiro, MA, Rinaldi, JC, et al. Gestational protein restriction delays prostate morphogenesis in male rats. Reprod Fertil Dev. 2014; 26, 967–973.Google Scholar
154. Wagenlehner, F, Pilatz, A, Linn, T, et al. Prostatitis and andrological implications. Minerva Urol Nefrol. 2013; 65, 117–123.Google Scholar
155. Ficarra, V, Rossanese, M, Zazzara, M, et al. The role of inflammation in lower urinary tract symptoms (LUTS) due to benign prostatic hyperplasia (BPH) and its potential impact on medical therapy. Curr Urol Rep . 2014; 15, 463–469.Google Scholar
156. Petry, CJ, Dorling, MW, Pawlak, DB, Ozanne, SE, Hales, CN. Diabetes in old male offspring of rat dams fed a reduced protein diet. Int J Exp Diabetes Res. 2001; 2, 139–143.Google Scholar
157. Martin-Gronert, MS, Ozanne, SE. Mechanisms linking suboptimal early nutrition and increased risk of type 2 diabetes and obesity. J Nutr. 2010; 140, 662–666.Google Scholar
158. Hales, C, Barker, D. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Int J Epidemiol. 2013; 42, 1215–1222.Google Scholar
159. Thurner, S, Klimek, P, Szell, M, et al. Quantification of excess risk for diabetes for those born in times of hunger, in an entire population of a nation, across a century. Proc Natl Acad Sci U SA. 2013; 110, 4703–4707.Google Scholar
160. Wang, N, Wang, X, Li, Q, et al. The famine exposure in early life and metabolic syndrome in adulthood. Clin Nutr. 2017; 36, 253–259.Google Scholar
161. Veldhuis, JD. Changes in pituitary function with ageing and implications for patient care. Nat Rev Endocrinol. 2013; 9, 205–215.Google Scholar
162. Dhindsa, S, Prabhakar, S, Sethi, M, et al. Frequent occurrence of hypogonadotropic hypogonadism in type 2 diabetes. J Clin Endocrinol Metabol. 2004; 89, 5462–5468.Google Scholar
163. Moretti, C, Lanzolla, G, Moretti, M, Gnessi, L, Carmina, E. Androgens and hypertension in men and women: a unifying view. Curr Hypertens Rep. 2017; 19, 44.Google Scholar
164. Fukui, M, Tanaka, M, Hasegawa, G, Yoshikawa, T, Nakamura, N. Association between serum bioavailable testosterone concentration and the ratio of glycated albumin to glycated hemoglobin in men with type 2 diabetes. Diabetes Care. 2008; 31, 397–401.Google Scholar
165. Schianca, GPC, Fra, GP, Brustia, F, et al. Testosterone plasma concentration is associated with insulin resistance in male hypertensive patients. Exp Clin Endocrinol Diabetes. 2017; 125, 171–175.Google Scholar
166. Burney, BO, Hayes, TG, Smiechowska, J, et al. Low testosterone levels and increased inflammatory markers in patients with cancer and relationship with cachexia. J Clin Endocrinol Metabol. 2012; 97, E700–E709.Google Scholar
167. Wickramatilake, CM, Mohideen, MR, Pathirana, C. Association of metabolic syndrome with testosterone and inflammation in men. Ann Endocrinol. 2015; 76, 260–263.Google Scholar
168. Reis, SRL, Feres, NH, Ignacio-Souza, LM, et al. Nutritional recovery with a soybean diet after weaning reduces lipogenesis but induces inflammation in the liver in adult rats exposed to protein restriction during intrauterine life and lactation. Mediators Inflamm. 2015; 2015, 781703.Google Scholar
169. Tarry-Adkins, JL, Fernandez-Twinn, DS, Hargreaves, IP, et al. Coenzyme Q10 prevents hepatic fibrosis, inflammation, and oxidative stress in a male rat model of poor maternal nutrition and accelerated postnatal growth. Am J Clin Nutr. 2016; 103, 579–588.Google Scholar
170. Barron, AM, Pike, CJ. Sex hormones, aging, and Alzheimer’s disease. Front Biosci. 2012; 4, 976–997.Google Scholar
171. Magnani, JW, Moser, CB, Murabito, JM, et al. Association of sex hormones, aging, and atrial fibrillation in men: the Framingham Heart Study. Circ Arrhythm Electrophysiol. 2014; 7, 307–312.Google Scholar
172. Sipilä, S, Narici, M, Kjaer, M, et al. Sex hormones and skeletal muscle weakness. Biogerontology. 2013; 14, 231–245.Google Scholar
173. Gann, PH, Hennekens, CH, Ma, J, Longcope, C, Stampfer, MJ. Prospective study of sex hormone levels and risk of prostate cancer. J Natl Cancer Inst. 1996; 88, 1118–1126.Google Scholar
174. Udensi, U, Tchounwou, P. Oxidative stress in prostate hyperplasia and carcinogenesis. J Exp Clin Cancer Res. 2016; 35, 139.Google Scholar
175. Khandrika, L, Kumar, B, Koul, S, Maroni, P, Koul, HK. Oxidative stress in prostate cancer. Cancer Lett. 2009; 282, 125–136.Google Scholar
176. Nelles, LJ, Hu, WY, Prins, GS. Estrogen action and prostate cancer. Expert Rev Endocrinol Metab. 2011; 6, 437–451.Google Scholar
177. Walsh, TJ, Schembri, M, Turek, PJ, et al. Increased risk of high-grade prostate cancer among infertile men. Cancer. 2010; 116, 2140–2147.Google Scholar
178. Tvrda, E, Agarwal, A, Alkuhaimi, N. Male reproductive cancer and infertility: a mutual relationship. Int J Mol Sci. 2015; 16, 7230–7260.Google Scholar
179. Hanson, BM, Eisenberg, ML, Hotaling, JM. Male Infertility: a biomarker of individual and familial cancer risk. Fertil Steril. 2018; 109, 6–9.Google Scholar
180. Skakkebaek, NE, Rajpert-De, ME, Buck, LGM, et al. Male reproductive disorders and fertility trends: influences of environment and genetic susceptibility. Physiol Rev. 2016; 96, 55–97.Google Scholar
181. Barker, DJP, Osmond, C, Thornburg, KL, Kajantie, E, Eriksson, JG. A possible link between the pubertal growth of girls and prostate cancer in their sons. Am J Hum Biol. 2012; 24, 406–410.Google Scholar
182. Bhutta, ZA, Haider, BA. Prenatal micronutrient supplementation: Are we there yet? Can Med Assoc J. 2009; 180, 1188–1189.Google Scholar