286 KC Caires, JA Schmidt, AP Oliver, J de Avila and DJ McLeanneonatal boar ages evaluated (Fig. 2e). This suggeststhat testosterone may directly or <strong>in</strong>directly regulate thehomeostasis of these cell types <strong>in</strong> the neonatal boartestis, potentially contribut<strong>in</strong>g to the observed donor agevariation <strong>in</strong> the establishment of spermatogenesis <strong>in</strong> thegraft<strong>in</strong>g study, and it is known that post-natal testisdevelopment is conserved between grafted and <strong>in</strong> vivotestis tissue (Oatley et al. 2004; Zeng et al. 2006).Our results demonstrate age-related differences <strong>in</strong> thepotential of neonatal testis tissue to grow and supportcomplete germ cell differentiation when grafted onimmunodeficient mice. More importantly, these f<strong>in</strong>d<strong>in</strong>gs<strong>in</strong>dicate important physiological changes <strong>in</strong> germ andSertoli cell homeostasis dur<strong>in</strong>g neonatal testis development<strong>in</strong> the boar, and may expla<strong>in</strong> why previousattempts to <strong>in</strong>crease testis size and sperm production<strong>in</strong> boars have been unsuccessful. This conclusion issupported by <strong>in</strong> vivo evidence (At-Taras et al. 2006,2008), and as a result we suggest future efforts to impactlifetime fertility <strong>in</strong> boars should occur dur<strong>in</strong>g the first2 weeks of neonatal life.From an application standpo<strong>in</strong>t, tissue orig<strong>in</strong>at<strong>in</strong>gfrom 14-day boar testis resulted <strong>in</strong> the greatest degree ofgraft germ cell differentiation; this stage <strong>in</strong> developmentmay be ideally suited for germ l<strong>in</strong>e genetic manipulationof cells, potentially facilitat<strong>in</strong>g a novel means to producetransgenic boar spermatozoa. Further, as Sertoli cellsprovide an immunoprotective barrier for develop<strong>in</strong>ggerm cells, neonatal porc<strong>in</strong>e Sertoli cells have seen<strong>in</strong>creas<strong>in</strong>g use to encapsulate porc<strong>in</strong>e islet cells prior totransplantation <strong>in</strong> human patients with diabetes mellitus(Dufour et al. 2003; Valdes-Gonzalez et al. 2007), andthus a better understand<strong>in</strong>g of the basic mechanismsregulat<strong>in</strong>g their homeostasis, and survival after transplantationis necessitated. We also demonstrated nodifferences <strong>in</strong> the ability of cryopreserved and freshlygrafted donor porc<strong>in</strong>e testis tissue to grow, producetestosterone and establish spermatogenesis. Thus, assomatic cell function is restored after freez<strong>in</strong>g, cryopreservationof pre-pubertal testis tissue prior to graft<strong>in</strong>gpresents a novel means for male germ l<strong>in</strong>epreservation. The factors regulat<strong>in</strong>g the biologicalactivity of Sertoli and germ cell homeostasis <strong>in</strong> theneonatal boar testis will be the focus of future experimentsand may provide <strong>in</strong>sights for both agriculturaland biomedical applications.AcknowledgementThis research was supported <strong>in</strong> part by a graduate research fellowshipprovided by the Seattle Chapter of the Achievement Rewards forCollege Scientists Foundation on behalf of K.C.C.ReferencesAlmeida FF, Leal MC, Franca LR, 2006: Testis morphometry,duration of spermatogenesis, and spermatogenic efficiency<strong>in</strong> the wild boar (Sus scrofa). Biol Reprod 75, 792–799.Amann RP, 1970: Sperm production rates. In: Johnson AD,Gomes WR, VanDemark NL (eds), The Testis, Vol. 1.Academic Press, New York, pp. 433–482.Arslan M, We<strong>in</strong>bauer GF, Schlatt S, Shahab M, Nieschlag E,1993: FSH and testosterone, alone or <strong>in</strong> comb<strong>in</strong>ation,<strong>in</strong>itiate testicular growth and <strong>in</strong>crease the number ofspermatogonia and Sertoli cells <strong>in</strong> a juvenile non-humanprimate (Macaca mulatta). J Endocr<strong>in</strong>ol 136, 235–243.At-Taras EE, Berger T, McCarthy MJ, Conley AJ, Nitta-OdaBJ, Roser JF, 2006: Reduc<strong>in</strong>g estrogen synthesis <strong>in</strong> develop<strong>in</strong>gboars <strong>in</strong>creases testis size and total sperm production.J Androl 27, 552–559.At-Taras EE, Kim IC, Berger T, Conley A, Roser JF, 2008:Reduc<strong>in</strong>g endogenous estrogen dur<strong>in</strong>g development altershormone production by porc<strong>in</strong>e Leydig cells and sem<strong>in</strong>iferoustubules. 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Biol Reprod 71, 494–501.Orth JM, 1984: The role of follicle-stimulat<strong>in</strong>g hormone <strong>in</strong>controll<strong>in</strong>g Sertoli cell proliferation <strong>in</strong> testes of fetal rats.Endocr<strong>in</strong>ology 115, 1248–1255.Orth JM, Gunsalus GL, Lamperti AA, 1988: Evidence fromSertoli cell-depleted rats <strong>in</strong>dicates that spermatid number<strong>in</strong> adults depends on numbers of Sertoli cells produceddur<strong>in</strong>g per<strong>in</strong>atal development. Endocr<strong>in</strong>ology 122, 787–794.Ó 2008 The Authors. Journal compilation Ó 2008 Blackwell Verlag
Endocr<strong>in</strong>e Regulation of Porc<strong>in</strong>e Spermatogenesis 287Padmanabhan V, Sharma TP, 2001: Neuroendocr<strong>in</strong>e vs.paracr<strong>in</strong>e control of follicle-stimulat<strong>in</strong>g hormone. ArchMed Res 32, 533–543.Parv<strong>in</strong>en M, Ventela S, 1999: Local regulation of spermatogenesis:a liv<strong>in</strong>g cell approach. Hum Fertil (Camb) 2, 138–142.Plant TM, Marshall GR, 2001: The functional significance ofFSH <strong>in</strong> spermatogenesis and the control of its secretion <strong>in</strong>male primates. Endocr Rev 22, 764–786.Ramaswamy S, Plant TM, Marshall GR, 2000: Pulsatilestimulation with recomb<strong>in</strong>ant s<strong>in</strong>gle cha<strong>in</strong> human lute<strong>in</strong>iz<strong>in</strong>ghormone elicits precocious sertoli cell proliferation <strong>in</strong> thejuvenile male rhesus monkey (Macaca mulatta). Biol Reprod63, 82–88.Russell LD, 1993: Form, dimensions and cytology of mammalianSertoli cells. In: Russell LD, Griswold MD (eds),The Sertoli Cell. Cache River Press, Clearwater, FL, pp.1–37.Russell LD, Ettl<strong>in</strong> RA, S<strong>in</strong>ha Hikim AP, Clegg ED, 1990:Mammalian spermatogenesis. <strong>in</strong>: Russell LD, Ettl<strong>in</strong> RA,S<strong>in</strong>ha Hikim AP, Clegg ED (eds), Histological and HistopathologicalEvaluation of the Testis. Cache River Press,Clearwater, FL, pp. 1–40.Schmidt JA, de Avila JM, McLean DJ, 2006: Graft<strong>in</strong>gperiod and donor age affect the potential for spermatogenesis<strong>in</strong> bov<strong>in</strong>e ectopic testis xenografts. Biol Reprod 75,160–166.Sharpe RM, Walker M, Millar MR, Atanassova N, Morris K,McK<strong>in</strong>nell C, Saunders PT, Fraser HM, 2000: Effect ofneonatal gonadotrop<strong>in</strong>-releas<strong>in</strong>g hormone antagonistadm<strong>in</strong>istration on Sertoli cell number and testicular development<strong>in</strong> the marmoset: comparison with the rat. BiolReprod 62, 1685–1693.Stosiek P, Kasper M, Karsten U, 1990: Expression of cytokerat<strong>in</strong>8 and 18 <strong>in</strong> human Sertoli cells of immature and atrophicsem<strong>in</strong>iferous tubules. Differentiation 43, 66–70.Valdes-Gonzalez RA, White DJ, Dorantes LM, Teran L,Garibay-Nieto GN, Bracho-Blanchet E, Davila-Perez R,Evia-Viscarra L, Ormsby CE, Ayala-Sumuano JT, Silva-Torres ML, Ramirez-Gonzalez B, 2007: Three-yr follow-upof a type 1 diabetes mellitus patient with an islet xenotransplant.Cl<strong>in</strong> Transplant 21, 352–357.Waites GM, Speight AC, Jenk<strong>in</strong>s N, 1985: The functionalmaturation of the Sertoli cell and Leydig cell <strong>in</strong> themammalian testis. J Reprod Fertil 75, 317–326.Yomogida K, Ohtani H, Harigae H, Ito E, Nishimune Y,Engel JD, Yamamoto M, 1994: Developmental stage- andspermatogenic cycle-specific expression of transcriptionfactor GATA-1 <strong>in</strong> mouse Sertoli cells. Development 120,1759–1766.Zarate A, Garrido J, Canales ES, Soria J, Schally AV, 1974:Disparity <strong>in</strong> the negative gonadal feedback control for LHand FSH secretion <strong>in</strong> cases of germ<strong>in</strong>al aplasia or Sertolicell-onlysyndrome. J Cl<strong>in</strong> Endocr<strong>in</strong>ol Metab 38, 1125–1127.Zeng W, Avelar GF, Rathi R, Franca LR, Dobr<strong>in</strong>ski I, 2006:The length of the spermatogenic cycle is conserved <strong>in</strong>porc<strong>in</strong>e and ov<strong>in</strong>e testis xenografts. J Androl 27, 527–533.Zirk<strong>in</strong> BR, 1998: Spermatogenesis: its regulation by testosteroneand FSH. Sem<strong>in</strong> Cell Dev Biol 9, 417–421.Author’s address (for correspondence): DJ McLean, Wash<strong>in</strong>gton StateUniversity, Pullman, Wash<strong>in</strong>gton, 99164–6353, USA. E-mail:dmclean@wsu.eduConflict of <strong>in</strong>terest: All authors declare no conflict of <strong>in</strong>terests.Ó 2008 The Authors. Journal compilation Ó 2008 Blackwell Verlag
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422 P Loi, K Matzukawa, G Ptak, Y N
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Table of Contents Volume 43 · Supp