High-lipid nutritional environment in different ontogenetic periods induce developmental programming of rat prostate at aging

in Reproduction
Authors:
Tatiane Pereira ScarpelliDepartament of Biological Sciences, São Paulo State University (UNESP), Institute of Biosciences, Humanities and Exact Sciences, São José do Rio Preto, São Paulo, Brazil

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Eloisa Zanin PytlowancivDepartament of Biological Sciences, São Paulo State University (UNESP), Institute of Biosciences, Humanities and Exact Sciences, São José do Rio Preto, São Paulo, Brazil
Department of Structural and Functional Biology, State University of Campinas (UNICAMP), Campinas, São Paulo, Brazil

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Maria Etelvina Pinto-FochiDepartament of Biological Sciences, São Paulo State University (UNESP), Institute of Biosciences, Humanities and Exact Sciences, São José do Rio Preto, São Paulo, Brazil
Faculdade de Medicina, União das Faculdades dos Grandes Lagos (UNILAGO), São José do Rio Preto, São Paulo, Brazil

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Sebastião Roberto TabogaDepartament of Biological Sciences, São Paulo State University (UNESP), Institute of Biosciences, Humanities and Exact Sciences, São José do Rio Preto, São Paulo, Brazil

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https://orcid.org/0000-0002-0970-4288
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Rejane Maira GóesDepartament of Biological Sciences, São Paulo State University (UNESP), Institute of Biosciences, Humanities and Exact Sciences, São José do Rio Preto, São Paulo, Brazil

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https://orcid.org/0000-0002-3622-460X

Correspondence should be addressed to R M Góes; Email: rejane.goes@unesp.br
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In brief

Maternal obesity plus high-fat diet in breastfeeding induces stromal hyperplasia and diffuse acinar atrophy in the rat prostate at aging, related to dyslipidemia and testosterone reduction. The high-lipid nutritional environment from intrauterine and throughout life favors the development of prostatic intraepithelial neoplasia and aggravated degenerative alterations in the gland.

Abstract

Maternal obesity and high-fat diet (HFD) affect permanently prostate histophysiology in adulthood, but the consequences during aging are unknown. Here, we evaluated the prostate alterations in middle-aged rats subjected to a high-lipid nutritional environment (HLE) in different ontogenetic periods. Wistar rats (56 weeks of age) were assigned into groups exposed to standard nutrition (C) or HLE during gestation (G), gestation and lactation (GL), from lactation onward (L), from weaning onward (W) and from gestation onward (AL). HLE in the periods after weaning consisted of HFD (20% fat), and during gestation and lactation it also included previous maternal obesity induced by the HFD. HLE increased total cholesterol and triglyceride levels in all groups and led to insulin resistance in GL and AL and obesity in L. Serum testosterone levels decreased ~67% in GL, ~146% in L and W, and ~233% in AL. Histological and stereological analysis revealed an increment of the stromal compartment and collagen fibers in the prostates of all HLE groups, as well as degenerative lesions, such as cell vacuolation and prostate concretions. HLE aggravated acinar atrophy in G, GL, and L, and in AL it reached more than 50% of the prostate area for most animals. The foci of prostatic intraepithelial neoplasia increased in AL. Tissue expression of androgen receptor did not vary among groups, except for a higher stromal expression for G and GL. Even when restricted to gestation and lactation, HLE induces diffuse acinar atrophy in the aging prostate and worsens degenerative and premalignant lesions when it continues throughout life.

 

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  • Agnoux AM, Antignac JP, Simard G, Poupeau G, Darmaun D, Parnet P & Alexandre-Gouabau MC 2014 Time window-dependent effect of perinatal maternal protein restriction on insulin sensitivity and energy substrate oxidation in adult male offspring. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 307 R184R197. (https://doi.org/10.1152/ajpregu.00015.2014)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Aki T, Nara A & Uemura K 2012 Cytoplasmic vacuolization during exposure to drugs and other substances. Cell Biology and Toxicology 28 125131. (https://doi.org/10.1007/s10565-012-9212-3)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Armitage JA, Taylor PD & Poston L 2005 Experimental models of developmental programming: consequences of exposure to an energy-rich diet during development. Journal of Physiology 565 38. (https://doi.org/10.1113/jphysiol.2004.079756)

    • Search Google Scholar
    • Export Citation
  • Benesh EC, Humphrey PA, Wang Q & Moley KH 2013 Maternal high-fat diet induces hyperproliferation and alters Pten/Akt signaling in prostates of offspring. Scientific Reports 3 3466. (https://doi.org/10.1038/srep03466)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Berman DM, Yang J & Epstein JI 2000 Foamy gland high-grade prostatic intraepithelial neoplasia. American Journal of Surgical Pathology 24 140144. (https://doi.org/10.1097/00000478-200001000-00018)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Bhatia-Gaur R, Donjacour AA, Sciavolino PJ, Kim M, Desai N, Young P, Norton CR, Gridley T, Cardiff RD & Cunha GR et al.1999 Roles for Nkx3.1 in prostate development and cancer. Genes and Development 13 966977. (https://doi.org/10.1101/gad.13.8.966)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Billis A 2010 Prostatic atrophy. Clinicopathological significance. International Brazilian Journal of Urology 36 401409. (https://doi.org/10.1590/s1677-55382010000400003)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Bostwick DG & & Cheng L 2012 Precursors of prostate cancer. Histopathology 60 427. (https://doi.org/10.1111/j.1365-2559.2011.04007.x)

  • Brodowski L, Büter W, Kohls F, Hillemanns P, Von Kaisenberg C & Dammann O 2019 Maternal overweight, inflammation and neurological consequences for the preterm child: results of the ELGAN study. Geburtshilfe und Frauenheilkunde 79 11761182. (https://doi.org/10.1055/a-0960-0939)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Campos-Silva P, Fernandes A, Costa W, Sampaio FJ & Gregorio B 2020 Fetal programming by high-fat diet promoted the decreased of the prostate in adult Wistar albino rats. Mechanisms of Development 164 103649. (https://doi.org/10.1016/j.mod.2020.103649)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Cannarella R, Condorelli RA, Barbagallo F, La Vignera S & Calogero AE 2021 Endocrinology of the aging prostate: current concepts. Frontiers in Endocrinology 12 554078. (https://doi.org/10.3389/fendo.2021.554078)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Creasy D, Bube A, De Rijk E, Kandori H, Kuwahara M, Masson R, Nolte T, Reams R, Regan K & Rehm S et al.2012 Proliferative and nonproliferative lesions of the rat and mouse male reproductive system. Toxicologic Pathology 40 (6 S upplement) 40S121S. (https://doi.org/10.1177/0192623312454337)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Cunha GR, Ricke W, Thomson A, Marker PC, Risbridger G, Hayward SW, Wang YZ, Donjacour AA & Kurita T 2004 Hormonal, cellular, and molecular regulation of normal and neoplastic prostatic development. Journal of Steroid Biochemistry and Molecular Biology 92 221236. (https://doi.org/10.1016/j.jsbmb.2004.10.017)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • De Jesus MM, Negrin AC, Taboga SR, Pinto-Fochi ME & Góes RM 2015 Histopathological alterations in the prostates of Mongolian gerbils exposed to a high-fat diet and di-n-butyl phthalate individually or in combination. Reproductive Toxicology 52 2639. (https://doi.org/10.1016/j.reprotox.2015.02.005)

    • Search Google Scholar
    • Export Citation
  • De Marzo AM, Marchi VL, Epstein JI & Nelson WG 1999 Proliferative inflammatory atrophy of the prostate: implications for prostatic carcinogenesis. American Journal of Pathology 155 19851992. (https://doi.org/10.1016/S0002-9440(1065517-4)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Desai M, Jellyman JK, Han G, Beall M, Lane RH & Ross MG 2014 Maternal obesity and high-fat diet program offspring metabolic syndrome. American Journal of Obstetrics and Gynecology 211 237.e1237.e237. (https://doi.org/10.1016/j.ajog.2014.03.025)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Devlin CM, Simms MS & Maitland NJ 2021 Benign prostatic hyperplasia – what do we know? BJU International 127 389399. (https://doi.org/10.1111/bju.15229)

  • Drake AJ & Reynolds RM 2010 Impact of maternal obesity on offspring obesity and cardiometabolic disease risk. Reproduction 140 387398. (https://doi.org/10.1530/REP-10-0077)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Dupre NC, Flavin R, Sfanos KS, Unger RH, To S, Gazeeva E, Fiorentino M, De Marzo AM, Rider JR & Mucci LA et al.2018 Corpora amylacea in prostatectomy tissue and associations with molecular, histological, and lifestyle factors. Prostate 78 11721180. (https://doi.org/10.1002/pros.23692)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Escobar EL, Gomes-Marcondes MC & Carvalho HF 2009 Dietary fatty acid quality affects AR and PPARgamma levels and prostate growth. Prostate 69 548558. (https://doi.org/10.1002/pros.20905)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Evagelidou EN, Kiortsis DN, Bairaktari ET, Giapros VI, Cholevas VK, Tzallas CS & Andronikou SK 2006 Lipid profile, glucose homeostasis, blood pressure, and obesityanthropometric markers in macrosomic offspring of nondiabetic mothers. Diabetes Care 29 11971201. (https://doi.org/10.2337/dc05-2401)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Freeland J, Crowell PD, Giafaglione JM, Boutros PC & Goldstein AS 2021 Aging of the progenitor cells that initiate prostate cancer. Cancer Letters 515 2835. (https://doi.org/10.1016/j.canlet.2021.05.014)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Fukabori Y, Nakano K, Ohyama A & Yamanaka H 1997 Stimulative effect of transforming growth factor-beta on collagen synthesis by human prostatic stromal cells in vitro. International Journal of Urology 4 597602. (https://doi.org/10.1111/j.1442-2042.1997.tb00316.x)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Furriel A, Campos-Silva P, Silva PCGP, Costa WS, Sampaio FJB & Gregório BM 2014 Diets rich in saturated and polyunsaturated fatty acids induce morphological alterations in the rat ventral prostate. PLoS ONE 9 e102876. (https://doi.org/10.1371/journal.pone.0102876)

    • Search Google Scholar
    • Export Citation
  • Haffner MC, Weier C, Xu MM, Vaghasia A, Gürel B, Gümüşkaya B, Esopi DM, Fedor H, Tan HL & Kulac I et al.2016 Molecular evidence that invasive adenocarcinoma can mimic prostatic intraepithelial neoplasia (PIN) and intraductal carcinoma through retrograde glandular colonization. Journal of Pathology 238 3141. (https://doi.org/10.1002/path.4628)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Isaacs JT 1987 Development and characteristics of the available animal model systems for the study of prostatic cancer. Progress in Clinical and Biological Research 239 513576.

    • Search Google Scholar
    • Export Citation
  • Jeyakumar SM, Lopamudra P, Padmini S, Balakrishna N, Iridharan NV & Vajreswari A 2009 Fatty acid desaturation index correlates with body mass and adiposity indices of obesity in Wistar NIN obese mutant rats, strains WNIN/Ob and WNIN/GR-Ob. Nutrition and Metabolism 6 27. (https://doi.org/10.1186/1743-7075-6-27)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Li M, Sloboda DM & Vickers MH 2011 Maternal obesity and developmental programming of metabolic disorders in offspring: evidence from animal models. Experimental Diabetes Research 2011 592408. (https://doi.org/10.1155/2011/592408)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lovegrove C, Ahmed K, Challacombe B, Khan MS, Popert R & Dasgupta P 2015 Systematic review of prostate cancer risk and association with consumption of fish and fish-oils: analysis of 495,321 participants. International Journal of Clinical Practice 69 87105. (https://doi.org/10.1111/ijcp.12514)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Madersbacher S, Sampson N & Culig Z 2019 Pathophysiology of benign prostatic hyperplasia and benign prostatic enlargement: a mini-review. Gerontology 65 458464. (https://doi.org/10.1159/000496289)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Mann S, Sidhu M & Gowin K 2020 Understanding the mechanisms of diet and outcomes in colon, prostate, and breast cancer; malignant gliomas; and cancer patients on immunotherapy. Nutrients 12 2226. (https://doi.org/10.3390/nu12082226)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Marker PC, Donjacour AA, Dahiya R & Cunha GR 2003 Hormonal cellular and molecular control of prostatic development. Developmental Biology 253 165174. (https://doi.org/10.1016/s0012-1606(0200031-3)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Mirzaei S, Paskeh MDA, Saghari Y, Zarrabi A, Hamblin MR, Entezari M, Hashemi M, Aref AR, Hushmandi K & Kumar AP et al.2022 Transforming growth factor-beta (TGF-β) in prostate cancer: a dual function mediator? International Journal of Biological Macromolecules 206 435452. (https://doi.org/10.1016/j.ijbiomac.2022.02.094)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Narita S, Nara T, Sato H, Koizumi A, Huang M, Inoue T & Habuchi T 2019 Research evidence on high-fat diet-induced prostate cancer development and progression. Journal of Clinical Medicine 8 597. (https://doi.org/10.3390/jcm8050597)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Nascimento AF, Sugizaki MM, Leopoldo AS, Lima-Leopoldo AP, Luvizotto RA, Nogueira CR & Cicogna AC 2008 A hypercaloric pellet-diet cycle induces obesity and co-morbidities in Wistar rats. Arquivos Brasileiros de Endocrinologia e Metabologia 52 968974. (https://doi.org/10.1590/s0004-27302008000600007)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Oben JA, Mouralidarane A, Samuelsson AM, Matthews PJ, Morgan ML, McKee C, Soeda J, Fernandez-Twinn DS, Martin-Gronert MS & Ozanne SE et al.2010 Maternal obesity during pregnancy and lactation programs the development of offspring non-alcoholic fatty liver disease in mice. Journal of Hepatology 52 913920. (https://doi.org/10.1016/j.jhep.2009.12.042)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ogden CL, Carroll MD, Kit BK & Flegal KM 2014 Prevalence of childhood and adult obesity in the United States, 2011–2012. JAMA 311 806814. (https://doi.org/10.1001/jama.2014.732)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Oliveira DSM, Dzinic S, Bonfil AI, Saliganan AD, Sheng S & Bonfil RD 2016 The mouse prostate: a basic anatomical and histological guideline. Bosnian Journal of Basic Medical Sciences 16 813. (https://doi.org/10.17305/bjbms.2016.917)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Osório-Costa F, Rocha GZ, Dias MM & Carvalheira JBC 2009 Epidemiological and molecular mechanisms aspects linking obesity and cancer. Arquivos Brasileiros de Endocrinologia e Metabologia 53 213226. (https://doi.org/10.1590/s0004-27302009000200013)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Pasquali R & Gambineri A 2006 Metabolic effects of obesity on reproduction. Reproductive Biomedicine Online 12 542551. (https://doi.org/10.1016/s1472-6483(1061179-0)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Picó C, Reis F, Egas C, Mathias P & Matafome P 2021 Lactation as a programming window for metabolic syndrome. European Journal of Clinical Investigation 51 e13482. (https://doi.org/10.1111/eci.13482)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Pinto-Fochi ME, Pytlowanciv EZ, Reame V, Rafacho A, Ribeiro DL, Taboga SR & Góes RM 2016 A high-fat diet fed during different periods of life impairssteroidogenesis of rat Leydig cells. Reproduction 152 795808. (https://doi.org/10.1530/REP-16-0072)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Pomerantz MM, Qiu X, Zhu Y, Takeda DY, Pan W, Baca SC, Gusev A, Korthauer KD, Severson TM & Ha G et al.2020 Prostate cancer reactivates developmental epigenomic programs during metastatic progression. Nature Genetics 52 790799. (https://doi.org/10.1038/s41588-020-0664-8)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Prins GS & Korach KS 2008 The role of estrogens and estrogen receptors in normal prostate growth and disease. Steroids 73 233244. (https://doi.org/10.1016/j.steroids.2007.10.013)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Pytlowanciv EZ, Pinto-Fochi ME, Reame V, Gobbo MG, Lisboa DL, Taboga SR & Góes RM 2016 Differential ontogenetic exposure to obesogenic environmentinduces hyperproliferative status and nuclear receptors unbalance in the rat prostate at adulthood. Prostate 76 662678. (https://doi.org/10.1002/pros.23158)

    • Search Google Scholar
    • Export Citation
  • Pytlowanciv EZ, Ribeiro DL, Tamarindo GH, Taboga SR & Góes RM 2022 High-fat diet during sexual maturation induces hyperplastic differentiation of rat prostate and higher expression of AR45 isoform and ERα. Reproductive Biology 22 100674. (https://doi.org/10.1016/j.repbio.2022.100674)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Rafacho A, Roma LP, Taboga SR, Boschero AC & Bosqueiro JR 2007 Dexamethasone-induced insulin resistance is associated with increased connexin 36 mRNA and protein expression in pancreatic rat islets. Canadian Journal of Physiology and Pharmacology 85 536545. (https://doi.org/10.1139/y07-037)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Rawla P 2019 Epidemiology of prostate cancer. World Journal of Oncology 10 6389. (https://doi.org/10.14740/wjon1191)

  • Reame V, Pytlowanciv EZ, Ribeiro DL, Pissolato TF, Taboga SR, Góes RM & Pinto-Fochi ME 2014 Obesogenic environment by excess of dietary fats in different phases of development reduces spermatic efficiency of Wistar rats at adulthood: correlations with metabolic status. Biology of Reproduction 91 151. (https://doi.org/10.1095/biolreprod.114.121962)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Rebello RJ, Oing C, Knudsen KE, Loeb S, Johnson DC, Reiter RE, Gillessen S, Van der Kwast T & Bristow RG 2021 Prostate cancer. Nature Reviews: Disease Primers 7 9. (https://doi.org/10.1038/s41572-020-00243-0)

    • Search Google Scholar
    • Export Citation
  • Ribeiro DL, Taboga SR & Góes RM 2009 Diabetes induces stromal remodeling andincreases in chondroitin sulphate proteoglycans of the rat ventral prostate. International Journal of Experimental Pathology 90 400411. (https://doi.org/10.1111/j.1365-2613.2009.00657.x)

    • Search Google Scholar
    • Export Citation
  • Ribeiro DL, Pinto ME, Rafacho A, Bosqueiro JR, Maeda SY, Anselmofranci JA, Taboga SR & Góes RM 2012a High-fat diet obesity associated with insulin resistance increases cell proliferation, estrogen receptor, and PI3K proteins in rat ventral prostate. Journal of Andrology 33 854865. (https://doi.org/10.2164/jandrol.111.016089)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ribeiro DL, Pinto ME, Maeda SY, Taboga SR & Góes RM 2012b High fat-induced obesity associated with insulin-resistance increases FGF-2 content and causes stromal hyperplasia in rat ventral prostate. Cell and Tissue Research 349 577588. (https://doi.org/10.1007/s00441-012-1420-x)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Röcken C, Linke RP & Saeger W 1996 Corpora amylacea in the lung, prostate and uterus. A comparative and immunohistochemical study. Pathology, Research and Practice 192 9981006. (https://doi.org/10.1016/S0344-0338(9680041-0)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Rosa-Ribeiro R, Barbosa GO, Kühne F & Carvalho HF 2014 Desquamation is a novel phenomenon for collective prostate epithelial cell deletion after castration. Histochemistry and Cell Biology 141 213220. (https://doi.org/10.1007/s00418-013-1152-3)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Sanches B, Tamarindo GH, Dos Santos Maldarine J, da Silva A, Dos Santos VA, Lima M, Rahal P, Góes RM, Taboga SR & Felisbino SL et al.2020 Telocytes contribute to aging-related modifications in the prostate. Scientific Reports 10 21392. (https://doi.org/10.1038/s41598-020-78532-7)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Scarano WR, Cordeiro RS, Góes RM, Carvalho HF & Taboga SR 2005 Tissueremodeling in guinea pig lateral prostate at different ages after estradiol treatment. Cell Biology International 29 778784. (https://doi.org/10.1016/j.cellbi.2005.05.003)

    • Search Google Scholar
    • Export Citation
  • Schauer IG & Rowley DR 2011 The functional role of reactive stroma in benign prostatic hyperplasia. Differentiation 82 200210. (https://doi.org/10.1016/j.diff.2011.05.007)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Sertie R, Kang M, Antipenko JP, Liu X, Maianu L, Habegger K & Garvey WT 2020 In utero nutritional stress as a cause of obesity: altered relationship between body fat, leptin levels and caloric intake in offspring into adulthood. Life Sciences 254 117764 (https://doi.org/10.1016/j.lfs.2020.117764)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Sfanos KS, Isaacs WB & De Marzo AM 2013 Infections and inflammation in prostate cancer. American Journal of Clinical and Experimental Urology 1 311.

  • Shah S, Jha B & Khanal MP 2011 Effects of aging and ethnicity on serum free prostate specific antigen. Asian Pacific Journal of Cancer Prevention 12 25092512. (available at: http://journal.waocp.org/?sid=Entrez:PubMed&id=pmid:22320948&key=2011.12.10.2509)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Shappell SB, Thomas GV, Roberts RL, Herbert R, Ittmann MM, Rubin MA, Humphrey PA, Sundberg JP, Rozengurt N & Barrios R et al.2004 Prostate pathology of GeneticallyEngineered mice: definitions and classification. The consensus report from the Bar Harbor meeting of the Mouse Models of Human Cancer Consortium Prostate Pathology Committee. Cancer Research 64 22702305. (https://doi.org/10.1158/0008-5472.can-03-0946)

    • Search Google Scholar
    • Export Citation
  • Shubin AV, Demidyuk IV, Komissarov AA, Rafieva LM & Kostrov SV 2016 Cytoplasmic vacuolization in cell death and survival. Oncotarget 7 5586355889. (https://doi.org/10.18632/oncotarget.10150)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Silva SA, Gobbo MG, Pinto-Fochi ME, Rafacho A, Taboga SR, Almeida EA, Góes RM & Ribeiro DL 2015 Prostate hyperplasia caused by long-term obesity is characterized by high deposition of extracellular matrix and increased content of MMP-9 and VEGF. International Journal of Experimental Pathology 96 2130. (https://doi.org/10.1111/iep.12107)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Sperandio S, Poksay K, De Belle I, Lafuente MJ, Liu B, Nasir J & Bredesen DE 2004 Paraptosis: mediation by MAP kinases and inhibition by AIP-1/Alix. Cell Death and Differentiation 11 10661075. (https://doi.org/10.1038/sj.cdd.4401465)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Stoykova GE & Schlaepfer IR 2019 Lipid metabolism and endocrine resistance in prostate cancer, and new opportunities for therapy. International Journal of Molecular Sciences 20 2626. (https://doi.org/10.3390/ijms20112626)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Sullivan EL & Grove KL 2010 Metabolic imprinting in obesity. Forum of Nutrition 63 186194. (https://doi.org/10.1159/000264406)

  • Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A & Bray F 2021 Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: A Cancer Journal for Clinicians 71 209249. (https://doi.org/10.3322/caac.21660)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Symonds ME 2007 Integration of physiological and molecular mechanisms of the developmental origins of adult disease: new concepts and insights. Proceedings of the Nutrition Society 66 442450. (https://doi.org/10.1017/S002966510700571X)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Tamarindo GH, Gobbo MG, Taboga SR, Almeida EA & Góes RM 2021 Melatonin ameliorates degenerative alterations caused by age in the rat prostate and mitigates high-fat diet damages. Cell Biology International 45 92106. (https://doi.org/10.1002/cbin.11472)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Taylor BA & Phillips SJ 1996 Detection of obesity Qtls on mouse chromosomes 1 and 7 by selective DNA pooling. Genomics 34 389398. (https://doi.org/10.1006/geno.1996.0302)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Thomson AA & Cunha GR 1999 Prostatic growth and development are regulated by FGF10. Development 126 36933701. (https://doi.org/10.1242/dev.126.16.3693)

  • Timms BG 2008 Prostate development: a historical perspective. Differentiation 76 565577. (https://doi.org/10.1111/j.1432-0436.2008.00278.x)

  • Toivanen R & Shen MM 2017 Prostate organogenesis: tissue induction, hormonal regulation and cell-type specification. Development 144 13821398. (https://doi.org/10.1242/dev.148270)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Vilamaior PSL, Taboga SR & Carvalho HF 2006 Postnatal growth of the ventral prostate in Wistar rats: a stereological and morphometrical study. Anatomical Record, Part A, Discoveries in Molecular, Cellular, and Evolutionary Biology 288 885892. (https://doi.org/10.1002/ar.a.20363)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Vuichoud C & Loughlin KR 2015 Benign prostatic hyperplasia: epidemiology, economics and evaluation. Canadian Journal of Urology 22 (Supplement 1) 16.

  • Walsh TJ 2011 Male reproductive health and prostate cancer risk. Current Opinion in Urology 21 506513. (https://doi.org/10.1097/MOU.0b013e32834bdf14)

  • Weibel ER, Kistler GS & Scherle WF 1966 Practical stereological methods formorphometric cytology. Journal of Cell Biology 30 2338. (https://doi.org/10.1083/jcb.30.1.23)

    • Search Google Scholar
    • Export Citation
  • World Health Organization (WHO) 2016 Obesity and overweight. In WHO Fact Sheets, n. 854. WHO.

  • Wright AS, Thomas LN, Douglas RC, Lazier CB & Rittmaster RS 1996 Relative potency of testosterone and dihydrotestosterone in preventing atrophy and apoptosis in the prostate of the castrated rat. Journal of Clinical Investigation 98 25582563. (https://doi.org/10.1172/JCI119074)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Yang T, Wu X, Hu J, Hu M, Xu H, Jiang H & Ding Q 2018 Maternal high-fat diet promotes the development and progression of prostate cancer in transgenic adenocarcinoma mouse prostate offspring. Cellular Physiology and Biochemistry 47 18621870. (https://doi.org/10.1159/000491066)

    • PubMed
    • Search Google Scholar
    • Export Citation